Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-10T13:00:13.792Z Has data issue: false hasContentIssue false
  • English
  • Français

Pigment granule migration in crustacean photoreceptors requires calcium

Published online by Cambridge University Press:  02 June 2009

Christina King-Smith  and
Thomas W. Cronin
Christina King-Smith
Affiliation:
Department of Biological Sciences, University of Maryland – Baltimore County, Baltimore
Thomas W. Cronin
Affiliation:
Department of Biological Sciences, University of Maryland – Baltimore County, Baltimore
Get access Rights & Permissions [Opens in a new window]

Abstract

We have investigated the role of calcium in the regulation of pigment granule migration in photoreceptors of the semi-terrestrial crab, Sesarma cinereum. Isolated crab eyes (eyecup plus eyestalk) were maintained in crustacean Ringer either prepared normally or calcium-free plus 50 mM EGTA. Pigment granule movement was indirectly observed by monitoring reflectance from the eye during light stimuli using intracellular optical physiological techniques. Electroretinograms (ERGs) were also measured during light stimuli. EGTA treatment caused gradual loss of centripetal migration of pigment granules (normally leading to pupillary closure), and photoreceptors eventually became locked in the open-pupil, dark-adapted state despite repeated stimuli. In contrast, ERG responses continued throughout EGTA treatment, although the size and shape ofthe response was altered. Normal ERG responses and pigment granule movements returned after replacing EGTA-Ringer with normal-calcium medium. These results suggest that centripetal migration of pigment granules in crustacean photoreceptors requires calcium.

Keywords

Pigment granule migrationInvertebrate photoreceptorsExtracellular calciumElectroretinogramIntracellular optical physiology
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 1 , January 1996 , pp. 43 - 49
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Arikawa, K., Hicks, J.L. & Williams, D.S. (1990). Identification of actin filaments in the rhabdomeral microvilli of Drosophila photoreceptors. Journal of Cell Biology 110, 1993–1998.Google Scholar
Autrum, H. (1981). Light and dark adaptation in invertebrates. In Handbook of Sensory Physiology, Vol. VII/6C: Comparative Physiology and Evolution of Vision in Invertebrates C: Invertebrate Visual Centers and Behavior–II, ed. Autrum, H., pp. 2–91. New York: Springer Verlag.Google Scholar
Baumann, O. (1992). Structural interactions of actin filaments and endoplasmic reticulum in honeybee photoreceptor cells. Cell and Tissue Research 268, 71–79.CrossRefGoogle Scholar
Bearer, E.L., DeGiorgis, J.A., Bodner, R.A., Kao, A.W. & Reese, T.S. (1993). Evidence for myosin motors on organelles in squid axo-plasm. Proceedings of the National Academy of Sciences of the U.S.A. 90, 11252–11256.Google Scholar
Bernard, C.D. & Stavenga, D.G. (1978). Spectral sensitivities of retinular cells measured in intact, living bumblebees by an optical method. Naturwissenschaften 65, 442–443.CrossRefGoogle Scholar
Blest, A.D., de Couet, H.G., Howard, J., Wilcox, M. & Sigmund, C. (1984). The extrarhabdomeral cytoskeleton in photoreceptors of Diptera. 1. Labile components in the cytoplasm. Proceedings of the Royal Society B (London) 220, 339–352.Google Scholar
Cavenaugh, G.M. (1956). Formulae and Methods of the Marine Biological Laboratory Chemical Room. Woods Hole, Massachusetts.Google Scholar
Cheney, R.E., O'Shea, M.K., Heuser, J.E., Coelho, M.V., Wolenski, J.S., Espreafico, E.M., Forscher, P., Larson, R.E. & Mooseker, M.S. (1993). Brain myosin-V is a two-headed unconventional myosin with motor activity [see comments]. Cell 75, 13–23.CrossRefGoogle ScholarPubMed
Collins, K., Sellers, J.R. & Matsudaira, P. (1990). Calmodulin dissociation regulates brush border myosin I (110–kD-calmodulin) mech-anochemical activity in vitro. Journal of Cell Biology 110, 1137–1147.CrossRefGoogle ScholarPubMed
Cosens, D.J. & Manning, A. (1969). Abnormal electroretinogram from a Drosophila mutant. Nature 224, 285–287.CrossRefGoogle ScholarPubMed
Cronin, T.W. & King, C.A. (1989). Spectral sensitivity in the mantis shrimp, Gonodactylus oerstedii, determined using noninvasive optical techniques. Biological Bulletin 176, 308–316.Google Scholar
Cronin, T.W. (1989). Application of intracellular optical techniques to the study of stomatopod crustacean vision. Journal of Comparative Physiology A 164, 737–749.Google Scholar
Endow, S.A. & Titus, M.A. (1992). Genetic approaches to molecular motors. Annual Review of Cell Biology 8, 29–66.Google Scholar
Frank, T.M. & Fein, A. (1991). The role of the inositol phosphate cascade in visual excitation of invertebrate microvillar photoreceptors. Journal of General Physiology 97, 697–723.CrossRefGoogle ScholarPubMed
Frixione, E. (1983). The microtubular system of crayfish retinula cells and its changes in relation to screeing pigment migration. Cell and Tissue Research 232, 335–348.Google Scholar
Frixione, E. & Aréchiga, H. (1981). Ionic dependence of screening pigment migrations in crayfish retinular photoreceptors. Journal of Comparative Physiology 144, 35–43.CrossRefGoogle Scholar
Frixione, E. & Ruiz, L. (1988). Calcium uptake by smooth endoplasmic reticulum of peeled retinal photoreceptors of the crayfish. Journal of Comparative Physiology A 162, 91–100.CrossRefGoogle Scholar
Goldstein, L.S.B. (1993). With apologies to Scheherazade: Tails of 1001 kinesin motors. Annual Review of Genetics 27, 319–351.Google Scholar
Hardie, R.C. & Minke, B. (1992). The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors. Neuron 8, 643–651.CrossRefGoogle ScholarPubMed
Hardie, R.C. & Minke, B. (1993). Novel Ca2+ channels underlying transduction in Drosophila photoreceptors: Implications for phos-phoinositide-mediated Ca2+ mobilization. Trends in Neuroscience 16, 371–376.Google Scholar
Hochstrate, P. & Hamdorf, K. (1985). The influence of extracellular calcium on the response of fly photoreceptors. Journal of Comparative Physiology 156, 53–64.Google Scholar
Hollenbeck, P.J. (1993). Phosphorylation of neuronal kinesin heavy and light chains in vivo. Journal of Neurochemistry 60, 2265–2275.Google Scholar
Howard, J. (1984). Calcium enables photoreceptor pigment migration in a mutant fly. Journal of Experimental Biology 113, 471–475.Google Scholar
King, C.A. & Cronin, T.W. (1994 a). Investigations of pigment granule transport systems in Gonodactylus oerstedii (Crustacea, Hoplocarida, Stomatopoda) 1. Effects of low temperature on the pupillary response. Journal of Comparative Physiology A 175, 323–329.Google Scholar
King, C.A. & Cronin, T.W. (1994 b). Investigations of pigment granule transport systems in Gonodactylus oerstedii (Crustacea, Hoplocarida, Stomatopoda) II. Effects of low temperature on pigment granule position and microtubule populations in retinular cells. Journal of Comparative Physiology A 175, 331–342.CrossRefGoogle Scholar
King, C.A. & Cronin, T.W. (1993). Cytoskeleton of retinular cells from thestomatopod, Gonodactylus oerstedii: Possible roles in pigment granule migration. Cell and Tissue Research 274, 315–328.CrossRefGoogle Scholar
Kirschfeld, K. & Franceschini, N. (1969). Ein Mechanismus zur Steurung des Lichtflusses in den Rhabdomeren des Komplexauges von Musca. Kybernetik 6, 13–22.Google Scholar
Kirschfeld, K. & Vogt, K. (1980). Calcium ions and pigment granule migration in fly photoreceptors. Naturwissenschaften 67, 516–517.CrossRefGoogle Scholar
Kotz, K.J. & McNiven, M.A. (1994). Intracellular calcium and cAMP regulate directional pigment movements in teleost erythrophores. Journal of Cell Biology 124, 463–474.CrossRefGoogle ScholarPubMed
Lin, S.X. & Collins, C.A. (1993). Regulation of the intracellular distribution of cytoplasmic dynein by serum factors and calcium. Journal of Cell Science 105, 579–588.Google Scholar
Lisman, J.E. & Brown, J.E. (1972). The effects of intracellular iontophoretic injection of calcium and sodium ions on the light response of Limulus ventral photoreceptors. Journal of General Physiology 59, 701–719.Google Scholar
Lisman, J.E. & Brown, J.E. (1975). Effects of intracellular injection of calcium buffers on light adaptation in Limulus ventral photoreceptors. Journal of General Physiology 66, 489–506.Google Scholar
Lo, M.V. & Pak, W.L. (1981). Light-induced pigment granule migration in the retinular cells of Drosophila melanogaster: Comparison of wild type with ERG-defective mutants. Journal of General Physiology 77, 155–175.Google Scholar
McNiven, M.A. & Ward, J.B. (1988). Calcium regulation of pigment transport in vitro. Journal of Cell Biology 106, 111–125.Google Scholar
Mermall, V., McNally, J.G. & Miller, K.G. (1994). Transport of cytoplasmic particles catalysed by an unconventional myosin in living Drosophila embryos. Nature 369, 560–562.Google Scholar
Miller, W.H. & Cawthon, D.F. (1974). Pigment granule movement in Limulus photoreceptors. Investigative Ophthalmology 13, 401–405.Google Scholar
Mondragón, R. & Frixione, E. (1992). Conditional inhibition of screening-pigment aggregation by lidocaine in crayfish photoreceptors and frog retinal pigment epithelium. Journal of Experimental Biology 166, 197–214.Google Scholar
Montell, C. & Rubin, G.R. (1989). Molecular characterization of the Drosophila trp locus: A putative integral membrane protein required for phototransduction. Neuron 2, 1313–1323.Google Scholar
Oshima, N., Hayakawa, M. & Sugimoto, M. (1990). The involvement of calmodulin in motile activities of fish chromatophores. Comparative Biochemistry and Physiology 97C, 33–36.Google Scholar
Oshima, N., Suzuki, M., Yamaji, N. & Fujii, R. (1988). Pigment aggregation is triggered by an increase in free calcium ions within fish chromatophores. Comparative Biochemistry and Physiology 91A, 27–32.Google Scholar
Payne, R., Corson, D.W., Fein, A. & Berridge, M.J. (1986). Excitation and adaptation of photoreceptors by inositol 1,4,5, trisphosphate results from a rise in intracellular calcium. Journal of General Physiology 88, 127–142.CrossRefGoogle ScholarPubMed
Payne, R. & Fein, A. (1987). Inositol 1,4,5, trisphosphate releases calcium from specialized sites within Limulus photoreceptors. Journal of Cell Biology 104, 933–937.Google Scholar
Payne, R., Walz, B., Levy, S. & Fein, A. (1988). The localization of calcium release by inositol trisphosphate in Limulus photoreceptors and its control by negative feedback. Philosophical Transactions of the Royal Society B (London) 320, 359–379.Google Scholar
Perrelet, A. & Bader, C. (1978). Morphological evidence for calcium stores in photoreceptors of the honeybee drone retina. Journal of Ultrastructural Research 63, 237–243.Google Scholar
Sammak, P.J., Adams, S.R., Harootunian, A.T., Schliwa, M. & Tsien, R.Y. (1992). Intracellular cyclic AMP not calcium determines the direction of vesicle movement in melanophores: Direct measurement by fluorescence ratio imaging. Journal of Cell Biology 117, 57–72.Google Scholar
Stavenga, D.G. & Kuiper, J.W. (1977). Insect pupil mechanisms I. On the pigment migration in the retinula cells of Hymenoptera (Suborder Apocrita). Journal of Comparative Physiology 113, 55–72.CrossRefGoogle Scholar
Thaler, C.D. & Haimo, L.T. (1990). Regulation of organelle transport in melanophores by calcineurin. Journal of Cell Biology 111, 1939–1948.Google Scholar
Walz, B. (1979). Subcellular localization and ATP-dependent Ca2+ uptake by smooth endoplasmic reticulum in an invertebrate photoreceptor cell. An ultrastructural, cytochemical and X-ray microanalytical study. European Journal of Cell Biology 20, 83–91.Google Scholar
Weyrauther, E. (1989). Requirements for screening pigment migration in the eye of Ephestia kuehniella Z. Journal of Insect Physiology 35, 925–934.Google Scholar
Wilcox, M. & Franceschini, N. (1984). Stimulated drug uptake in a photoreceptor cell. Neuroscience Letters 50, 187–192.CrossRefGoogle Scholar
Zuidervaart, H., Stavenga, D.G., Stark, W.S. & Bernard, G.D. (1979). Pupillary responses revealing receptor characteristics in wild-type and mutant Drosophila. Society for Neuroscience Abstracts 5, 814.Google Scholar